Surveillance of travellers has historically focused on tourists, people visiting friends and relatives or those returning from business trips. These areas of travel remain significant, but international events in the past two years have given rise to noteworthy developments. From the beginning of the West African Ebola virus disease (EVD) outbreak at the end 2013, there has been an enhanced emphasis on protection of the Scottish population from imported viral haemorrhagic fever (VHF). While travel from affected areas was restricted due to actions by the World Health Organization (WHO) and airlines, the focus was on risk management of those travellers who were involved in supporting the response. HPS participated in monitoring the health of volunteers returning from the three main affected countries as well as responding to the challenges raised by the diagnosis of a case of EVD in Glasgow in the closing days of 2014.1
From a European perspective the ongoing mass immigration of people from Africa and the Middle East has also presented surveillance challenges. The focus here is on the consequences to public health caused by infrastructure failure resulting in the re-emergence of serious infectious diseases in this population.2 However, it is generally recognised that this effect is likely to be minor compared to the negative health impacts caused by the affects of pre-, peri- and post-migration events on migrants themselves.3
The risk of infection in travellers varies with destination, point of origin and type of travel.4, 5 Travel-related illnesses are not limited to the exotic: travellers may encounter infections abroad which are also found at home, where the risk of exposure is different or reduced. Fever and acute diarrhoea are common6 and it has been noted that travellers to developing countries are often affected by gastrointestinal infections and by respiratory infections.7 Skin disorders are also commonly reported8, 9 Disease may also be observed in those arriving from permanent residence abroad, as exemplified by a proportion of imported malaria diagnosed in Scotland.10
Infections acquired during travel may have the potential for transmission in transit or when the traveller arrives home or at another destination, although the risks are limited by effective public health measures. Effective surveillance of travel-related infection informs provision of evidence-based health advice to the traveller11 and also contributes to protection of the domestic population from imported pathogens. Scotland, in common with the rest of the United Kingdom has rigorous procedures for the management of those individuals diagnosed with serious infectious diseases, including viral haemorrhagic fever.
In this report we summarise 1) recent travel trends as a context and 2) laboratory notifications of travel-related significance.
Travel abroad 2000 - 2014
Travel from the UK
Travel from the UK grew steadily from the start of the millennium but fell in 2008/2009, declining to 55.6 million journeys in 2010. Since that point, numbers have gradually increased to 60.1 million in 2014.12 Travel to North America from the UK has declined between 2000 and 2014, while for Asia the numbers have risen since 2010. There has been a decrease in travel to Africa since 2008 while travel to Latin America and the Caribbean has been steady.
Of 60.1 million foreign visits by UK residents in 2014, most (78%) were to Europe, with another 6%, 5%, 4%, 2% and 2% of journeys to North America, Asia, Africa, and Latin America & Caribbean and the Middle East respectively. Travel to Australia and New Zealand accounted for 1% of foreign visits. From 2010 to 2014, holiday travel has seen an average annual growth of 1.4%. Business travel has increased annually by 0.4%. The largest increase is in visiting friends or relatives (VFR) which has grown, on average, by 5.2% between 2010 and 2014.
Travel from Scotland
In 2014, there were 3.9 million journeys abroad from Scotland, an increase of 6% from the previous year, representing 6% of total journeys from the UK. Europe (78%) was the most visited destination followed by North America (8%), Asia (4%), Africa (3%), Latin America & Caribbean (2%), the Middle East (2%) and Australia & New Zealand (1%). Apart from a slight increase in travel to North America and Middle East, these proportions are similar to those recorded in 2014.
Surveillance of travel-related infections
Results of positive laboratory tests for a wide variety of pathogens are received at Health Protection Scotland by electronic transfer through ECOSS.13 Clinical diagnoses are only received by ECOSS if they have been recorded in supporting text with the laboratory result. The data for 2015 for selected organisms were collated, episode criteria checked and duplicates removed.
It is assumed that infections such as schistosomiasis, vector-borne viruses, trypanosomiasis and leishmaniasis are always travel-related when they are identified in Scotland. Infections that can also be transmitted in the UK are only classified as imported when the appropriate information is recorded in the ECOSS report.
Escherichia coli O157, viral hepatitis and malaria figures for 2015 will be reported elsewhere.
The number of reports for the various organisms was broadly similar to that published in 2014. All reports are subject to review and results presented here may be revised in future publications of this or other HPS reports.
There were 195 episodes of Giardia in 2015, of which 38 (19%) were reported as imported. In 2014 there were 167 episodes, of which 36 (22%) were reported as imported. 742 episodes of Cryptosporidium included 64 (9%) which were imported. The total for 2014 was 431, of which 31 (7%) were imported. Three episodes of Entamoeba histolytica were reported in 2015, all of which were imported. In 2014, there were 11 episodes of E. histolytica, again all imported. Eight (33%) of 24 episodes of Cyclospora were recorded as imported. In 2014 there were two episodes of Cyclospora infection, of which one was reported as imported.
Nine episodes of enteric fever were reported to HPS in 2015, a decrease compared to 2014 when there were 20 episodes. The 2015 total comprised one Salmonella Paratyphi A, one S. Paratyphi B and seven S. Typhi. Both of the S. Paratyphi were reported as imported, as were six (86%) episodes of S. Typhi. In 2014, there were 12 S. Paratyphi A all of which were imported and eight S. Typhi, of which four (50%) were recorded as imported.
In 2015 there were seven episodes of Rickettsia, including one Rickettsia prowazekii, all of which were recorded as imported, compared to six episodes of Rickettsia in 2014, all of which were also imported.
HPS received reports of 111 Shigella episodes HPS in 2015, compared to 90 in 2013. Of those reported in 2015, there were 70 Shigella sonnei, 29 episodes of S. flexneri, eight of S.boydi and two of S. dysenteriae. Two episodes of Shigella were unspeciated. Fifty percent of Shigella episodes were imported in 2015 compared to 24% in 2014.
Seven Vibrio episodes were reported in 2015 compared to five in 2014. These comprised five Vibrio parahaemolyticus and two untyped V. cholerae. All Vibrio episodes in 2015 were imported, as was the case with the five episodes in 2014.
All vector-borne viruses reported in Scotland were imported. There were 30 episodes of dengue virus in 2015, compared to 29 in 2014. The number of episodes of chikungunya virus fell to three in 2015, with five having been reported in 2014. There were three episodes of West Nile virus in 2014, compared to two in 2014. There was one episode of yellow fever virus in 2015, with no previous episodes recorded in recent years.
In 2015, 133 episodes of Schistosoma infection were reported. These included five Schistosoma haematobium and one S. mansoni, the remaining 128 episodes being unspeciated. In 2014, there were 203 episodes of Schistosoma infection, of which one was S. haematobium and the remainder unspeciated.
Three episodes of Leishmania were reported in 2015. Of these, one was Leishmania viannia, one was L. braziliensis and one unspeciated. There was also one report of Trypanosoma cruzi. All of these were reported as imported. There were no reports of vector-borne protozoa in 2014.
This report considers only those infections where a specimen was tested or examined. Test results alone do not indicate the extent to which the patient was unwell as some positive results may relate to patients who were tested on a precautionary basis, e.g. for schistosomiasis, without having experienced symptoms of illness. HPS receives no indication of how many short-lived infections are acquired abroad but resolve before arrival in Scotland. The incubation period of some infections is short, so people may become ill quickly and recover before returning to this country. Thus, taken in isolation from other recording systems, ECOSS data does not accurately estimate total levels of disease in the travelling population.
As in previous years, organisms causing traveller’s diarrhoea (TD)14 are predominant in the reports. Salmonella, Shigella and Giardia are all familiar causes of TD with the last more often seen in longer-term travellers.15 An outbreak of cyclosporiasis occurred in Europe and North America in 2015 with UK episodes being linked to travel to Mexico.16 However, gastrointestinal infections are often acquired in Scotland and elsewhere in the UK without any stated link to international travel.
For some pathogens e.g. flaviviruses,17, 18, 19 a positive test result may arise from vaccination or cross-reaction. Occasionally, individuals will test positive for more than one pathogen. Clinical and travel histories are often absent from laboratory reports. In all circumstances, surveillance benefits from effective communication between epidemiologists and physicians.
Once again, dengue virus is the most frequently-reported vector-borne virus in Scotland. Dengue occurs across the tropics and is increasingly found in warmer areas of the temperate zone, transmission being reported in metropolitan France in 2010,20 201321 and 2015.22 Chikungunya virus has a range similar to dengue and is transmitted by the same Aedes sp mosquito vectors, although only three episodes were reported in Scotland in 2015. Major outbreaks of dengue and chikungunya have been ongoing in the Caribbean and the Americas for the past three years23,24 with Asia and the Pacific region also experiencing a significant burden of disease.25 In some countries these viruses have now supplanted malaria as the most significant vector-borne disease.
Zika virus, another flavivirus transmitted by Aedes mosquitoes, has spread across a similar range to that of dengue and chikungunya in the last two years, although no episodes have been reported in Scotland. In particular, Zika virus has spread rapidly through Brazil and neighbouring countries. It is suggested that Zika virus is the cause of a sharp increase in the incidence of microcephaly in newborns in Brazil.26 The evidence for a role in microcephaly is circumstantial, although an increase in similar birth defects was seen in French Polynesia following a Zika outbreak in 2014.27 Despite these concerns, Zika virus disease is generally a mild illness, having a similar clinical presentation to dengue, but symptoms generally less severe. There is no vaccine and no specific treatment is indicated.
There were been three reports of West Nile virus in Scotland in 2015, compared to two in 2014. While the infection can have serious clinical consequences, those infected do not pose a public health risk as viraemia is short lived28 and does not rise to a level necessary for transmission via the mosquito vector.29 West Nile virus is well established in southern, central and eastern Europe, with case numbers fluctuating annually.30
Many of the most common vector-borne viral infections share a clinical picture of fever, nausea, joint pain, myalgia and rash. Overlapping geographic ranges of viruses adds to the difficulty of differential diagnosis. Severe dengue and yellow fever meet the criteria for viral haemorrhagic fever (VHF). Consequently, it is essential that they can be distinguished from other VHFs such as Ebola virus disease. Although a dengue vaccine has now been licensed in Mexico, the Philippines and Brazil,31 the most important method of preventing mosquito-borne viral infection is rigorous bite avoidance.32 In this regard, avoidance of Zika virus with its uncertain consequences is as essential as for other potentially serious mosquito-borne viruses where no vaccine is available.
Schistosomiasis has been transmitted in France recently, with Schistosoma haematobium identified in Corsica in 2014 following diagnosis in travellers who had been swimming in the Cavu river system.33 This surprising development shows that infections can occur unexpectedly in travellers returning from destinations not commonly associated with serious health risks.
In the main, schistosomiasis affects travellers exposed in historically endemic areas, although reported episodes in Scotland have fallen sharply in number in 2015. Visits to Malawi by Scottish school students are frequent and may increase the risk of exposure to schistosomiasis and other infections.34 All schools planning travel abroad are encouraged to follow appropriate guidance.35 Worm burdens are usually low in travellers with infrequent exposure, meaning symptoms are usually absent or trivial. However, the risk of bladder carcinoma is uncertain, so those who may have been exposed through water contact are encouraged to seek testing. Diagnosis of infection by microscopy is rare, hence the infrequent speciation of schistosomiasis indentified in Scotland: diagnosis is by serology in nearly all cases.36
Small numbers of potentially serious infections including cutaneous diphtheria and louse-borne relapsing fever have been observed in migrant populations arriving in Europe in 2015.37 While these infections are a matter of public health concern in migrant camps and receiving centres, it is expected that normal sanitation and public health measures will continue to minimise the incidence and spread of imported infections in Europe. However, clinicians seeing patients who have arrived as migrants are encouraged to consider the possibility of unfamiliar infections and ensure patients are adequately protected against vaccine-preventable infection. Malaria and diverse helminth infections are common in sub-Saharan Africa and may occur in migrants arriving from that region. Leishmaniasis, of which there were three episodes in Scotland in 2015, may also be seen in migrants arriving from the Middle East and Africa.
Although not considered a new episode of infection, there was a single, well-publicised late neurological complication of Ebola virus disease in 2015, in a patient who had previously recovered from the disease. The long-term implication of this is uncertain, but it is possible that surveillance systems will be required to cope with apparently healthy individuals who unexpectedly become unwell on arrival from countries where EVD is present.
Organisms associated with traveller’s diarrhoea were most frequently reported in 2015, food and water hygiene remaining the most appropriate methods for reducing the risk from these infections. Some foodborne and waterborne diseases e.g. hepatitis A, typhoid and poliomyelitis are also preventable through vaccination. While vector-borne infections were less frequently reported, they continue to highlight the need for rigorous bite avoidance and vaccination where possible and appropriate. The possibility that Zika virus may have serious consequences for the developing fetus means that pregnant travellers should be especially conscientious in avoiding mosquito bites in areas where the virus is present.
Travel-related infections often manifest during or soon after travel, but may present months or years later, depending on the organism. Any traveller becoming unwell, even long after arrival in Scotland, should seek medical advice and report their travel history to their health care provider. It is recommended that anyone who may have been exposed to Schistosoma cercariae during travel is tested on their return, even if asymptomatic.38 HPS encourages all clinicians requesting laboratory testing for infectious disease to take a travel history, including travel several months previously, and to provide this information on the laboratory request form. This would allow HPS to report more accurately on the occurrence of travel-related infections in Scotland.
It is important to diagnose and treat infectious disease in newly-arrived travellers promptly and appropriately and in so doing improve the health of the patient and preserve public health. In this regard, the health of travellers and the health of resident populations are not considered to be entirely separate issues. In the context of migration, health professionals seeing newly arrived migrants presenting with infectious disease are encouraged to liaise appropriately with laboratory staff, infectious disease clinicians and health protection teams.
Up-to-date, expert advice on travel health and country-by-country disease risks is available to healthcare professionals on TRAVAX (http://www.travax.nhs.uk). Travellers are strongly advised to consult the fitfortravel website (http://www.fitfortravel.nhs.uk) in advance of their journey for information on how to stay healthy abroad. The website includes country-specific advice on recommended vaccines and antimalarial chemoprophylaxis, and details on safe food and water, accident avoidance, sun protection and insect bite avoidance. TRAVAX recommends that travellers consult a GP, practice nurse or travel health clinic at least six weeks before travel.39
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- European Centre for Disease Prevention and Control. Infectious diseases of specific relevance to newly-arrived migrants in the EU/EEA. ECDC Technical document. Available from: http://ecdc.europa.eu/en/publications/_layouts/forms/Publication_DispForm.aspx?List=4f55ad51-4aed-4d32-b960-af70113dbb90&ID=1405. (accessed 15 January 2016).
- European Centre for Disease Prevention and Control. Expert opinion on the public health needs of irregular migrants, refugees or asylum seekers across the EU’s southern and south-eastern borders. Available from: http://ecdc.europa.eu/en/publications/_layouts/forms/Publication_DispForm.aspx?List=4f55ad51-4aed-4d32-b960-af70113dbb90&ID=1377. (accessed 15 January 2016).
- Pistone T, Ezzedine K, Gaudin AF et al. Malaria prevention behaviour and risk awareness in French adult travellers. Travel Medicine & Infectious Disease. 2010;8:13-21. Available from: http://www.travelmedicinejournal.com/article/S1477-8939(09)00156-2/abstract. (accessed 15 January 2016).
- Centres for Disease Control and Prevention. Yellow Book 2014, Chapter 2. Available from: http://wwwnc.cdc.gov/travel/yellowbook/2014/chapter-2-the-pre-travel-consultation/perspectives-risks-travelers-face. (accessed 15 January 2016).
- Munro J, Redman C, Smith C et al. Report on GeoSentinel data collected at the Brownlee Centre for Infectious & Communicable Diseases, April 2011 – March 2013. HPS Weekly Report. 2014;48(2014/44):571-582. Available from: http://www.hps.scot.nhs.uk/ewr/redirect.aspx?id=61343. (accessed 15 January 2016).
- Redman CA, MacLennan A, Wilson E et al. Diarrhea and respiratory symptoms among travelers to Asia, Africa and South & Central America from Scotland. Journal of Travel Medicine. 2006;13:203-211. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16884402. (accessed 15 January 2016).
- Freedman DO, Weld LH, Kozarsky PE et al. Spectrum of disease and relation to place of exposure among ill travelers. New England Journal of Medicine. 2006;354:119-130. Available from: http://www.nejm.org/doi/full/10.1056/NEJMoa051331#t=articleResults. (accessed 15 January 2016).
- Gautret P, Schlagenhauf P, Gaudart J et al for the GeoSentinel Surveillance Network. Multicenter EuroTravNet/GeoSentinel study of travel-related infectious diseases in Europe. Emerging Infectious Diseases 2009;15(11):1783-1790. Available from: http://wwwnc.cdc.gov/eid/article/15/11/09-1147_article.htm. (accessed 15 January 2016).
- Munro J, Smith V, Smith C and Redman C. Travel health: Malaria in Scotland and the UK: 2010-2014. HPS Weekly Report 2014;49(2015/30):279-292. Available from: http://www.hps.scot.nhs.uk/ewr/redirect.aspx?id=64696. (accessed 15 January 2016).
- Fitfortravel. Disease Prevention Advice. 2013. Available from: http://www.fitfortravel.nhs.uk/advice.aspx#disease-prevention-advice. (accessed 15 January 2016).
- United Kingdom Office for National Statistics. Data and commentary from Travel Trends, 2014. Available from: http://www.ons.gov.uk/ons/publications/re-reference-tables.html?edition=tcm%3A77-391781. (accessed 15 January 2016).
- Wiuff C, Eastaway A, Tabbner C and Wayne B. Improved national disease surveillance through electronic communication of surveillance in Scotland (ECOSS). HPS Publications. 01/06/2007. Available from: http://www.hps.scot.nhs.uk/pubs/redirect.aspx?id=34706. (accessed 15 January 2016).
- Hill DR. Management of travellers’ diarrhoea BMJ. 2008;337:a1746. Available from: http://www.bmj.com/content/337/bmj.a1746.long. (accessed 15 January 2016).
- Gautret P, Cramer JP, Field V et al. Infectious diseases among travellers and migrants in Europe, EuroTravNet 2010. Eurosurveillance 2012;17(26):16-26. Available from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20205. (accessed 15 January 2016).
- Nichols GL, Freedman J, Pollock KG, Rumble C et al. Cyclospora infection linked to travel to Mexico, June to September 2015 Eurosurveillance 2015,20,(43):2-5. Available from: http://www.eurosurveillance.org/Public/Articles/Archives.aspx?PublicationId=11856. (accessed 15 January 2016).
- Koraka P, Zeller H, Niedrig M et al. Reactivity of serum samples from patients with a flavivirus infection measured by immunofluorescence assay and ELISA. Microbes and Infection. 2002;4(12):1209–1215. Available from: http://www.sciencedirect.com/science/article/pii/S1286457902016477. (accessed 15 January 2016).
- Peeling RW, Artsob H, Pelegrino JL et al. Evaluation of diagnostic tests: dengue. Nature Reviews Microbiology. 2010;December:S30-S37. Available from: http://www.nature.com/nrmicro/journal/v8/n12_supp/full/nrmicro2459.html. (accessed 15 January 2016).
- Mansfield KL, Horton DL, Johnson N et al. Flavivirus-induced antibody crossreactivity. Journal of General Virology. 2011;92:2821–2829. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3352572/. (accessed 15 January 2016).
- La Ruche G, Souarès Y, Armengaud A et al. First two autochthonous dengue virus infections in metropolitan France, September 2010. Eurosurveillance. 2010;15(39):pii=19676.Available from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19676. (accessed 15 January 2016).
- Marchand E, Prat C, Jeannin C, Lafont E et al Autochthonous case of dengue in France, October 2013. Eurosurveillance. 2013;18(50):pii=20661. Available from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20661. (accessed 15 January 2016).
- European Centre for Disease Prevention and Control. Communicable disease threats report, 20-26 September 2015, week 39. Available from: http://ecdc.europa.eu/en/press/news/_layouts/forms/News_DispForm.aspx?ID=1289&List=8db7286c-fe2d-476c-9133-18ff4cb1b568&Source=http%3A%2F%2Fecdc%2Eeuropa%2Eeu%2Fen%2Fpress%2Fnews%2FPages%2FNews%2Easpx%3Fp%3D4. (accessed 16 January 2016).
- PAHO/WHO. Annual Cases Reported of Dengue. Available from: http://www.paho.org/hq/index.php?option=com_topics&view=rdmore&cid=6290&Itemid=40734&lang=en. (accessed 15 January 2016).
- PAHO/WHO. Chikungunya. Available from: http://www.paho.org/hq/index.php?option=com_topics&view=article&id=343&Itemid=40931&lang=en. (accessed 15 January 2016).
- WHO/PRO Dengue situation updates. Available from: http://www.wpro.who.int/emerging_diseases/DengueSituationUpdates/en/. (accessed 15 January 2016).
- PAHO/WHO. Increase of microcephaly in the northeast of Brazil - Epidemiological Alert. 17/11/2015. Available from: http://www.paho.org/hq/index.php?option=com_docman&task=doc_download&Itemid=&gid=32636&lang=en. (accessed 16 January 2016).
- European Centre for Disease Prevention and Control. Epidemiological update: Complications potentially linked to the Zika virus outbreak, Brazil and French Polynesia. 27/11/2015. Available from: http://ecdc.europa.eu/en/press/news/_layouts/forms/News_DispForm.aspx?ID=1332&List=8db7286c-fe2d-476c-9133-18ff4cb1b568&Source=http%3A%2F%2Fecdc.europa.eu%2Fen%2FPages%2Fhome.aspx. (accessed 15 January 2016).
- Papa A, Danis K, Baka A et al. Ongoing outbreak of West Nile virus infections in humans in Greece, July-August 2010. Eurosurveillance. 2010;15(34):pii=19644. Available from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19644. (accessed 15 January 2016).
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- Fitfortravel. Insect bite avoidance. Available from: http://www.fitfortravel.nhs.uk/advice/general-travel-health-advice/insect-bite-avoidance.aspx. (accessed 16 January 2016).
- European Centre for Disease Prevention and Control. Rapid risk assessment: Local transmission of Schistosoma haematobium in Corsica, France. First update. Available from: http://ecdc.europa.eu/en/publications/_layouts/forms/Publication_DispForm.aspx?List=4f55ad51-4aed-4d32-b960-af70113dbb90&ID=1333. (accessed 16 January 2016).
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- Redman C, Spence G, Smith H and Smith K. Travel medicine: Schistosomiasis in Scotland 2005-2009; Laboratory confirmed ‘imported infections’, to week 53, 2009 & 2008. HPS Weekly Report. 2010;44(2010/03):24-26. Available from: http://www.hps.scot.nhs.uk/ewr/redirect.aspx?id=43726. (accessed 15 January 2016).
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